Pyrolysis temperature and time of rice husk biochar potentially control ammonia emissions and Chinese cabbage yield from urea-fertilized soils

Current agricultural practices are increasingly favoring the biochar application to sequester carbon, enhance crop growth, and mitigate various environmental pollutants resulting from nitrogen (N) loss. However, since biochar’s characteristics can vary depending on pyrolysis conditions, it is essential to determine the optimal standard, as they can have different effects on soil health. In this study, we categorized rice husk biochars basis on their pH levels and investigated the role of each rice husk biochar in reducing ammonia (NH3) emissions and promoting the growth of Chinese cabbage in urea-fertilized fields. The findings of this study revealed that the variation in pyrolysis conditions of rice husk biochars and N rates affected both the NH3 emissions and crop growth. The neutral (pH 7.10) biochar exhibited effective NH3 volatilization reduction, attributed to its high surface area (6.49 m2 g−1), outperforming the acidic (pH 6.10) and basic (pH 11.01) biochars, particularly under high N rates (640 kg N ha−1). Chinese cabbage yield was highest, reaching 4.00 kg plant−1, with the basic biochar application with high N rates. Therefore, the neutral rice husk biochar effectively mitigate the NH3 emissions from urea-treated fields, while the agronomic performance of Chinese cabbage enhanced in all biochar amendments.

Given the increasing focus on sustainable ecosystems and eco-friendly agriculture, contemporary agricultural practices encounter several challenges 1 .These challenges include the necessity to reduce the use of chemical fertilizers and pesticides, adopt minimal tillage techniques, incorporate organic amendments (e.g., organic fertilizer, manure compost, and biochar), and effectively manage nutrient lossess 1,2 .Specifically, the continuous and excessive application of nutrients, such as nitrogen (N) and phosphorus (P), through chemical fertilization can result in various environmental contaminations 2 .These contaminations involve the release of particulate matter (PM), greenhouse gases (GHGs), eutrophication, and algal bloom in both the atmosphere and aquatic ecosystems [3][4][5] .Ammonia (NH 3 ) volatilization stands out as a prominent source of N losses and contributes to the formation of secondary PM (PM 2.5 ) and nitrous oxide (N 2 O) 2,4,5 .Furthermore, NH 3 emissions has detrimental effects on air quality 5 , human health 4,6 , and the Earth's radiative balance 2 .These pollutants further exacerbate the impacts of global warming and climate change 5 .
Numerous studies have been dedicated to the development of sustainable and eco-friendly agricultural practices with the aim of reducing N losses, particularly NH 3 , while simultaneously enhancing crop productivity [7][8][9][10] .These practices encompass a range of approaches, including the application of natural urease inhibitors 2,3 , the introduction of elemental sulfur and polymers 9 , the use of organic fertilizer 4 , and the incorporation of biochar amendments 7,9,10 .Biochar, a carbon-rich material, is obtained through the pyrolysis of agricultural residues, biomass, and organic waste ingredients under relatively high temperatures and oxygen-limited conditions 7,[9][10][11][12] .It has garnered attention for its distinctive characteristics, such as carbon (C) sequestration 7,13 , promotion of plant growth 14,15 , enhancement of soil pH 4 , optimization of soil health 12 , provision of a habitat for microorganisms 13 , and the adsorption of heavy metals and nutrient contents 4,16 .Furthermore, biochar has the ability to absorb organic N, ammonium ions (NH 4 + ), and gaseous NH 3 through its functional groups and microspores, resulting in reduced N losses 15 .These properties of biochar are evident in the reduced N loss observed in agricultural soils treated with N fertilizers in the presence of biochar 17 .Unfortunately, many experiments have focused on the combined effects of several substitutes, such as urease inhibitor 2,18,19 , wood vinegar 20 , zeolite 21 , and compost 22,23 , or have explored the influence of biochar's formulation 24 and feedstock sources 25 on NH 3 emissions in agricultural soil.This variation in results may be attributed to the diverse characteristics of biochar produced under different pyrolysis conditions.Therefore, further studies are necessary to assess the efficiency of NH 3 emission reduction by biochar, taking into account biochar characteristics such as pH and surface area, which are related to N adsorption capacity.
We hypothesize that (1) higher pH levels in rice husk biochar might increase soil pH, hypothetically affecting NH 3 mitigation efficiency, and (2) excessive N rates could disturb Chinese cabbage yield.To assess these hypotheses, this study evaluated NH 3 volatilization and crop yield in a Chinese cabbage field treated with different rates of N fertilizer and three types of rice husk biochar classified based on their pH levels.The rice husk biochars were categorized as acidic (AB, pH 6.10), neutral (NB, pH 7.10), and basic (BB, pH 11.01), while N rates applied as urea were designed as N 0.5 (160 kg N ha −1 ), N 1.0 (320 kg N ha −1 , the recommended N rate), and N 2.0 (640 kg N ha −1 ), respectively.Results revealed that both NH 3 mitigation efficiency by the rice husk biochars and Chinese cabbage yield increased with rising N rates from 160 to 640 kg N ha −1 .Interestingly, NH 3 emissions from N fertilization were lowest in the soil treated with NB, which had the highest surface area compared to AB and BB.Due to the conflicting influences between BB's alkali effect and urea's pH-reducing impact, the N 0.5 treatment exhibited higher soil pH than the N 2.0 treatment, and soil chemical properties except for soil pH did not reach negative levels in the N 2.0 treatment.These unexpected findings suggest that the NH 3 mitigation rate primarily depended on the rice husk biochar's surface area rather than their pH values.Moreover, there was no negative effect in crop yield caused by excessive N supply owing to higher initial soil pH and the increased NH 3 emissions.

Pyrolysis conditions affect the characteristics of the rice husk biochar
Table 1 presents the chemical properties of the rice husk biochars and their corresponding pyrolysis conditions.The variations in pyrolysis temperature and time had a significant impact on the chemical properties of the rice husk biochar.The pH of the rice husk biochar exhibited a sharp increase as the pyrolysis temperature and time were raised from 400 to 600 °C and from 15 to 30 min, respectively.In contrast, the electrical conductivity (EC) values of AB, NB, and BB gradually decreased with the increase in their pyrolysis conditions.The surface area (SA) of the rice husk biochars was the highest in NB at 6.49 m 2 g −1 , while AB and BB were observed at 2.55 and 5.30 m 2 g −1 , respectively.The total carbon (TC) content of BB was significantly higher at 54.90% compared to 41.30% of AB and 44.10% of NB, while the total nitrogen (TN) content did not show a statistically significant difference among AB, NB, and BB.Conversely, the total hydrogen (TH) and total oxygen (TO) contents decreased with the increase in pyrolysis conditions and were the highest values in AB at 5.39 and 34.61%, respectively.Inorganic contents of the rice husk biochar gradually increased with the increased in pyrolysis conditions.The H:C and O:C ratio, which represent the aromaticity and polarity of the rice husk biochar, were higher at lower temperatures and shorter times.
The results of the analysis of functional groups on the surface of the rice husk biochar using Fourier transform infrared spectroscopy (FT-IR) were presented in Fig. 1.The secondary amide group, indicated by the -NH bond in the range of 3300-3325 cm −1 , was observed in NB and BB but not in AB.The C=C, -CH 3 , and -C-CN bonds in the range of 1640-1660 cm −1 , 1000-1050 cm −1 , and 400-420 cm −1 , respectively, were strongly formed with the increased pyrolysis conditions.

Ammonia volatilization reduce effectively by the neutral rice husk biochar
Figure 2 displays the daily NH 3 volatilization resulting from different N rates and rice husk biochar amendments.The NH 3 emissions peaked within 7 days after N application, with the first top-dressing fertilization leading to the maximum NH 3 release compared to the basal and other top-dressing fertilizations.Furthermore, the NH 3 peaks were higher with increasing the N rates (Fig. 3).The AB + N 2.0 treatment recorded the highest peak value at 20,127.94 g ha −1 day −1 (20.13 kg ha −1 day −1 ), while the NB + N 2.0 and BB + N 2.0 treatments reached 16,300.87(16.30kg ha −1 day −1 ) and 13,847.16g ha −1 day −1 (13.85 kg ha −1 day −1 ), respectively.After reaching the highest peak, the NH 3 volatilization sharply decreased and became similar to the control with non-N fertilization.
Figure 4 illustrates the total NH 3 emissions during the Chinese cabbage cropping season.The total NH 3 emissions were influenced by the N rates, and the reduction efficiency on NH 3 emission varied depending on the pH of the rice husk biochar (Supplementary Table S1).Cumulative NH 3 emissions were the lowest in NB treatments, such as NB + N 0.5 , NB + N 1.0 , and NB + N 2.0 , at 28.42, 42.99, and 108.54 kg ha −1 , respectively.In contrast, the only-urea treatments (i.e., N 0.5 , N 1.0 , and N 2.0 ) had the highest values at 38.64, 66.70, and 142.42 kg ha −1 , respectively.In comparison to the soil treated with basic rice husk biochar, the soil treated with acidic rice husk biochar exhibited lower NH 3 emissions, resulting in reductions of total NH 3 emissions by 6, 8, and 7% with varying N rates (N 0.5 , N 1.0 , and N 2.0 ).Moreover, the reductions in the total NH 3 emissions attributed to the rice husk biochar amendments were more pronounced with higher N rates, from N 0.5 to N 2.0 , effectively mitigating the N losses.The highest reduction efficiency by the rice husk biochar was shown in the NB + N 1.0 treatment at 36% compared to the N 1.0 treatment.Table 1.Chemical characteristics of rice husk biochar produced from different pyrolysis conditions.AB acidic (pH 6.1) rice husk biochar; NB neutral (pH 7.1) rice husk biochar; BB basic (pH 11.0) rice husk biochar; EC electrical conductivity, TC total carbon, TN total nitrogen, TH total hydrogen, TO total oxygen, T-P total phosphorus.

Growth of Chinese cabbage increases the N rates and the pH of the rice husk biochar
Table 3 presents the growth characteristics of Chinese cabbage influenced by the varying N rates and rice husk biochar amendments.The BB + N 2.0 treatment achieved the highest fresh weight at 4.00 kg plant −1 , while the N 2.0 , AB + N 2.0 , and NB + N 2.0 treatments yielded 3.40, 3.63, and 3.89 kg plant −1 , respectively.Additionally, fresh weight increased with the rising N rates and the pH of the rice husk biochar from N 0.5 to N 2.0 and from pH 6.10 to pH 11.01, respectively (Supplementary Table S2).However, the moisture contents of each treatment did not exhibit statistical significant difference.Head height and width were the highest in the BB + N 2.0 treatment, measuring 25.87 and 16.70 cm, respectively.Head growth increased with the increase in the N rates and the pH of the rice husk biochar.Furthermore, leaf length and width were higher with increasing the N rates and the pH of rice husk biochar, but statistically significant differences were observed only in the control treatment.The chlorophyll and TN content of Chinese cabbage were the highest in NB + N 0.5 and AB + N 1.0 , with SPAD values of 35.19 and a TN content of 3.71%, respectively, although they exhibited a non-specific trend.

Soil chemical properties change the N rates and the properties of the rice husk biochar
The soil chemical properties were influenced by both the N rates and the pH of the rice husk biochar (Table 2).Soil pH decreased as the N rates increased from 160 kg N ha −1 (N 0.5 ) to 640 kg N ha −1 (N 2.0 ), while soil EC increased.Furthermore, among the rice husk biochar amendments, soil pH increased with the rise in the pH of rice husk biochar.The EC values of the soil treated with AB, NB, and BB were lower than those of treatments  www.nature.com/scientificreports/with only urea (i.e., N 0.5 , N 1.0 , and N 2.0 ).The highest soil pH and EC were observed at pH 7.48 in BB + N 0.5 and 1.26 dS m −1 in N 2.0 , respectively.The rice husk biochar amendments effectively increased soil TC and TN contents compared to treatments with only urea.For instance, the co-application of BB and N 2.0 yielded the highest TC content at 2.36%, while the individual treatments of N 0.5 , N 1.0 , and N 2.0 decreased from the initial soil pH value of 0.71% to 0.61, 0.66, and 0.64%, respectively.In contrast, soil TN content increased with N fertilization, although no statistically significant difference was observed.Soil available nitrogen (Avail.N) content increased with the rice husk biochar amendment, with NB effectively increasing the Avail.N content under the same N rates conditions.In contrast, there were no significant differences observed in available phosphorus (Avail.P) content of N-treated soil (e.g., N 0.5 , N 1.0 , AB + N 0.5 , NB + N 1.0 , and BB + N 2.0 ).The highest Avail.P content was recorded in BB + N 1.0 at 125.05 mg kg −1 , while the Avail.P content of initial soil and control was 94.10 and 89.26 mg kg −1 , respectively.After rice husk biochar amendment and N fertilization, the content of exchangeable cations, such as Ca 2+ , K + , Mg 2+ , and Na + , increased, but no statistically significant difference was observed.

Discussion
Numerous prior studies have consistently shown that an increase in pyrolysis temperature results in heightened parameters such as pH, surface area, cation exchange capacity, and carbon content of biochar 26,27 .Particularly, the escalation in biochar pH predominantly arises from carbonate formation and the elevation in inorganic alkali contents 28,29 .Furthermore, the pH of biochar increases owing to presence of ash content and oxygen functional groups 30 .However, the composition of cellulose and hemicellulose in plant-based ingredients occurs at relatively low temperature (between 200 and 300 °C) and generate various organic acids and phenolic substances that decrease the pH of the material 30 .This implies that biochar produced at lower temperature might exhibit a lower pH compared to the initial raw material.On the other hand, the TH, and TO contents of rice husk biochars  Previous studies have reported that higher pyrolysis conditions lead to an increase in the proportion of nonvolatile compounds, particularly aromatic substances 31,32 .As the content of aromatic substances rises, the fixed www.nature.com/scientificreports/carbon content and non-volatile compounds in rice husk biochar increase, contributing to the enhancement of its stability and aromaticity 32 .Furthermore, the aforementioned parameters were also decreased by the TC content of rice husk biochar, showing a positive (+) correlation with pyrolysis conditions.The NH 3 emissions from agricultural soils are potentially depended on several factors such as the presence of soil amendments, the pH and moisture content of agricultural soil, method of nitrogen fertilizer application, and various agricultural practice (e.g., tillage, irrigation duration, and soil mulching) 4,33,34 .The PCA results by Liu et al. 35 were indicated that NH 3 volatilization varied in a descending order as follow: soil type, N source, soil pH, soil environmental conditions (e.g., temperature and moisture content).The application of biochar can adjust soil pH and enhance soil drainage, thereby improving the soil environment, which may influence NH 3 emissions 10,36 .Previous studies reported results indicating that biochar amendments promote the NH 3 emissions from agricultural soil owing to their alkali effects, which increase the soil pH [36][37][38] .In particular, high soil pH leads to higher rates of NH 3 volatilization because it raises the NH 3 concentrations dissolved in soil moisture 39 .Furthermore, another study documented that total NH 3 emissions increased by 10 to 71% with higher application rates of biochar 40 .These studies primarily focused on changes in soil pH influenced by the pH of biochar, and the NH 3 losses were found to be more pronounced in soil pH levels between 7 and 8 41 .To effectively manage the NH 3 emissions from agricultural land, it is necessary to maintain the soil pH below 7.0.
Conversely, several previous studies, which yielded conflicting results compared to the aforementioned studies, indicated that biochar amendments can effectively reduce the NH 3 volatilization from urea-treated soil under various conditions 42,43 .They demonstrated that the functional groups on the surface, adsorption ability, and cation exchange capacity of biochar contribute to decreasing NH 3 emissions from N-fertilized agricultural soils [44][45][46] .In this study, the soil amended with AB, NB, and BB exhibited lower NH 3 emissions compared to the solely urea-treated soil, which had the lowest soil pH values.These findings suggest that the reduction efficiency of NH 3 emissions by rice husk biochars, attributed to their functional groups, microspores, and adsorption ability, outweighs the increase in NH 3 emissions associated with elevated soil pH values.Furthermore, the reduction efficiency of rice husk biochars varied based on their pH, with BB amendment exhibiting higher NH 3 emissions compared to AB and NB amendments.As the pyrolysis conditions increased, the functional groups of BB decreased (Fig. 1), indicating a potential decrease in the NH 3 reduction efficiency of BB.This reduction could lead to a relatively higher NH 3 emissions, particularly when compared to AB or NB amendments, emphasizing the impact of pyrolysis conditions on the ammonia reduction efficiency of the biochar.
The application of rice husk biochars has been proven to enhance the growth and N uptake of Chinese cabbage, as shown in Table 3.This is supported by several previous studies that have examined the relationship between plant growth and biochar amendment 47 .Crop growth is primarily influenced by soil health, and biochar amendments are one of the factors that improve soil properties, fertility, and quality 48 .For instance, Munoz et al. 47 illustrated that biochar amendments can reduce both soil bulk density and particle density, while Peake et al. 48demonstrated that the application of biochar improves soil compaction by more than 10%.Additionally, biochar application enhances soil fertility as it supplies essential elements such as N, P, K, Ca, Mg, Fe, and Si 48 .The findings of this study also support the notion that soil nutrient contents (e.g., Avail.N and Avail.P) were increased by rice husk biochar amendments (Table 2).The application of rice husk biochars increased the soil Avail.N content by capturing gaseous NH 3 and NH 4 + through their functional groups.Nitrogen fixation by biochar was achieved through the surface characteristics of the biochar, primarily characterized by a negative charge 10 .The biochar absorbed N in cationic from (i.e., NH 4 + ), and it exhibited superiority with a large surface area.In this study, the application of NB (6.49 m 2 g −1 ), which had a larger surface area compared to AB (2.55 m 2 g −1 ) and BB (5.30 m 2 g −1 ), resulted in the highest Avail.N content in the N-fertilized soil under the same N rates condition (Table 2).However, since the ionic bond between the biochar surface and the cationic form of N needs to be disconnected for N uptake by plants, the fixed N was not immediately utilized by plants in the short term.These reasons supported our findings, which demonstrated the highest fresh weight of Chinese cabbage in the short-term cultivation experiment with BB amendment, not NB amendment, attributed to the higher soil OM content.Although, not showing statistically significant differences among AB, NB, and BB amendments, the NB application may still improve soil fertility over the long term, resulting in better crop yields.

Conclusions
This study demonstrates the significant impact of rice husk biochar amendments in mitigating the NH 3 emissions during the Chinese cabbage cropping period.The NH 3 emissions resulting from chemical fertilization in agricultural soil decreased in the presence of rice husk biochar.Notably, the neutral (pH 7.10) rice husk biochar amendment exhibited the most substantial reduction in the NH 3 volatilization compared to the acidic (pH 6.10) and basic (pH 11.01) rice husk biochars.Furthermore, biochar amendments improved the Chinese cabbage yield, and this improvement was more pronounced with an increase in the pH of rice husk biochar.The highest agronomic performance of Chinese cabbage was observed in the basic rice husk biochar treatment with the 640 kg N ha −1 (N 2.0 ).Therefore, the application of neutral rice husk biochar can effectively reduce the NH 3 emissions from N-fertilized agricultural soil, while basic rice husk biochar leads to the highest agronomic performance and yield of Chinese cabbage.

Experimental site
This study was conducted at the experimental field located in Chungnam National University, Daejeon, South Korea (35° 14′ 12.8″ N, 139° 7′ 0.5″ E).The experimental area experiences a humid continental and subtropical climate, both of which are influenced by the East Asian Monsoon

Preparation of rice husk biochar
The rice husk biochars were prepared under different pyrolysis conditions using an electrical furnace (1100 °C Box Furnace, Thermo Scientific Inc., Waltham, Massachusetts, USA).Initially, rice husks sourced from rice paddy at Chungnam National University underwent thorough washing with deionized water to eliminate several impurities (e.g., bird poop, insect corpse, soil, and crop residue).Subsequently, the damp rice husks were stored in a glass greenhouse for 2-week to remove their moisture content.Following this, the dried samples were placed in a stainless-steel barrel (Ø 260 × 140 mm) with and aluminum packing, and subjected to pyrolysis using an electrical furnace.In this study, the aluminum packing was used to block the oxygen (O 2 ) inflow.Finally, the rice husk biochars were categorized based on their pH values, specifically pH 6.1 (AB), pH 7.1 (NB), and pH 11.0 (BB).AB was produced at 350 °C for 15 min, while NB and BB were manufactured at 450 °C for 15 min and 600 °C for 30 min, respectively.The selected pyrolysis conditions were established based on prior studies 15 , that delineated the chemical properties of rice husk biochar under varying pyrolysis conditions, and preliminary experiment (Supplementary Table S3).In this study, AB exhibited the relatively minor differences from NB, likely attributed to the initial pH of the rice husk (pH 6.27).However, BB showed discernible differences from NB with increasing pyrolysis conditions.Therefore, we extended the pyrolysis time for BB from 15 to 30 min to observed the effect of stark pH differences.

Cultivation experiment
The cultivation experiment spanned a duration of 80 days, from April 12 to Jun 30, 2021, and followed a randomized complete block design with three replications.The 'Chunkwang' variety of Chinese cabbage (Brassica rapa L.) was sown in each plot, covering an area of 2.5 m × 3.0 m (7.5 m 2 ) with two rows.This study comprised thirteen treatments, including the following: control (non-fertilization), N fertilizer applied at recommended rate (320 kg N ha −1 , N 1.0 ), N fertilizer applied at half the recommended rate (160 kg N ha −1 , N 0.5 ), and N fertilizer applied at double the recommended rate (640 kg N ha −1 , N 2.0 ), as well as combined applications of the rice husk biochars (i.e., AB, NB, and BB) with N fertilizers (i.e., AB + N 1.0 , AB + N 0.5 , AB + N 2.0 , NB + N 1.0 , NB + N 0.5 , NB + N 2.0 , BB + N 1.0 , BB + N 0.5 , and BB + N 2.0 ).The rice husk biochars were applied to the agricultural soil at a rate of 1% (w w −1 ), which was recommended by previous studies 49 , and a mechanical tiller was used to incorporate the rice husk biochars with the soil.Before transplanting, 78 kg P 2 O 5 ha −1 , and 60 kg K 2 O ha −1 , in the form of fused phosphate and potassium chloride, respectively, were applied as basal fertilizer.Additionally, 46 kg K 2 O ha −1 of potassium chloride was applied at 15, 30, and 45 days after transplanting.Similarly, 55, 110, and 220 kg N ha −1 , in the form of urea, were applied as basal fertilizer, with 35, 70, and 140 kg N ha −1 applied in three installments during the cultivation period.The plots were irrigated every 2 days and after each fertilizer application to prevent water stress.

Ammonia measurement and analysis
The measurement of daily and total NH 3 emissions during the Chinese cabbage cultivation period was conducted using a static chamber made of acrylic material (h: 30 × Ø: 12 cm, 0.011 m 2 ) 24 .To capture the released NH 3 , a sponge soaked in a glycerol-phosphoric acid solution was placed inside the chamber for 24 h.Collection of https://doi.org/10.1038/s41598-024-54307-2www.nature.com/scientificreports/

Figure 1 .
Figure 1.FT-IR spectrum of rice husk biochars categorized by their pH values.

Figure 2 .
Figure 2. Daily NH 3 volatilization effected by different nitrogen rates and three types of rice husk biochar during the Chinese cabbage cropping period.N 0.5 , N 1.0 , and N 2.0 exhibited nitrogen application rates equivalent to 160 kg N ha −1 , 320 kg N ha −1 , and 640 kg N ha −1 , respectively, while AB, NB, and BB donated the acidic (pH 6.1), neutral (pH 7.1), and basic (pH 11.0) rice husk biochars.

Figure 3 .
Figure 3. Correlation between nitrogen rates and total NH 3 volatilization.

Figure 5 .
Figure 5.The meteorological data during the Chinses cabbage cultivation.
× D i )
a -fEach value with different letters within a column are significantly different from each other as determined by Duncan's multiple range test (p < 0.05).

Table 3 .
Growth characteristics of Chinese cabbage affected by the pH of rice husk biochar and different TreatmentsFresh weight (

kg plant −1 ) Moisture content (%) Head Leaf TN (%) Height (cm) Width (cm) Length (cm) Width (cm)
Vol.:(0123456789) Scientific Reports | (2024) 14:5692 | https://doi.org/10.1038/s41598-024-54307-2 4. During the summer season, which typically begins in June or July, the area receives high precipitation and is occasionally affected by typhoons.Detailed meteorological conditions during the cultivation period are presented in Fig.5.The experimental field had been conventionally used for cultivating Chinese cabbage for approximately 5-year.The soil in the experimental field is classified as sandy loam, consisting of 12.8% clay, 41.4% silt, and 45.8% sand, and it belongs to the Inceptisols order.